Effects of food supplementation and helminth removal on space use and spatial overlap in wild rodent populations.

Animal space use and spatial overlap can have important consequences for population-level processes such as social interactions and pathogen transmission. Identifying how environmental variability and inter-individual variation affect spatial patterns and in turn influence interactions in animal populations is a priority for the study of animal behaviour and disease ecology. Environmental food availability and macroparasite infection are common drivers of variation, but there are few experimental studies investigating how they affect spatial patterns of wildlife. Bank voles (Clethrionomys glareolus) are a tractable study system to investigate spatial patterns of wildlife and are amenable to experimental manipulations. We conducted a replicated, factorial field experiment in which we provided supplementary food and removed helminths in vole populations in natural forest habitat and monitored vole space use and spatial overlap using capture-mark-recapture methods. Using network analysis, we quantified vole space use and spatial overlap. We compared the effects of food supplementation and helminth removal and investigated the impacts of season, sex and reproductive status on space use and spatial overlap. We found that food supplementation decreased vole space use while helminth removal increased space use. Space use also varied by sex, reproductive status and season. Spatial overlap was similar between treatments despite up to threefold differences in population size. By quantifying the spatial effects of food availability and macroparasite infection on wildlife populations, we demonstrate the potential for space use and population density to trade-off and maintain consistent spatial overlap in wildlife populations. This has important implications for spatial processes in wildlife including pathogen transmission.

Extreme heat reduces host and parasite performance in a butterfly-parasite interaction.

Environmental temperature fundamentally shapes insect physiology, fitness and interactions with parasites. Differential climate warming effects on host versus parasite biology could exacerbate or inhibit parasite transmission, with far-reaching implications for pollination services, biocontrol and human health. Here, we experimentally test how controlled temperatures influence multiple components of host and parasite fitness in monarch butterflies (Danaus plexippus) and their protozoan parasites Ophryocystis elektroscirrha. Using five constant-temperature treatments spanning 18-34°C, we measured monarch development, survival, size, immune function and parasite infection status and intensity. Monarch size and survival declined sharply at the hottest temperature (34°C), as did infection probability, suggesting that extreme heat decreases both host and parasite performance. The lack of infection at 34°C was not due to greater host immunity or faster host development but could instead reflect the thermal limits of parasite invasion and within-host replication. In the context of ongoing climate change, temperature increases above current thermal maxima could reduce the fitness of both monarchs and their parasites, with lower infection rates potentially balancing negative impacts of extreme heat on future monarch abundance and distribution.

Enabling synthesis in fragment-based drug discovery (FBDD): microscale high-throughput optimisation of the medicinal chemist's toolbox reactions.

Miniaturised high-throughput experimentation (HTE) is widely employed in industrial and academic laboratories for rapid reaction optimisation using material-limited, multifactorial reaction condition screening. In fragment-based drug discovery (FBDD), common toolbox reactions such as the Suzuki-Miyaura and Buchwald-Hartwig cross couplings can be hampered by the fragment's intrinsic heteroatom-rich pharmacophore which is required for ligand-protein binding. At Astex, we are using microscale HTE to speed up reaction optimisation and prevent target down-prioritisation. By identifying catalyst/base/solvent combinations which tolerate unprotected heteroatoms we can rapidly optimise key cross-couplings and expedite route design by avoiding superfluous protecting group manipulations. However, HTE requires extensive upfront training, and this modern automated synthesis technique largely differs to the way organic chemists are traditionally trained. To make HTE accessible to all our synthetic chemists we have developed a semi-automated workflow enabled by pre-made 96-well screening kits, rapid analytical methods and in-house software development, which is empowering chemists at Astex to run HTE screens independently with minimal training.

Genomic analysis of the population structure of Paenibacillus larvae in New Zealand.

New Zealand is a remote country in the South Pacific Ocean. The isolation and relatively late arrival of humans into New Zealand has meant there is a recorded history of the introduction of domestic species. Honey bees (Apis mellifera) were introduced to New Zealand in 1839, and the disease American foulbrood was subsequently found in the 1870s. Paenibacillus larvae, the causative agent of American foulbrood, has been genome sequenced in other countries. We sequenced the genomes of P. larvae obtained from 164 New Zealand apiaries where American foulbrood was identified in symptomatic hives during visual inspection. Multi-locus sequencing typing (MLST) revealed the dominant sequence type to be ST18, with this clonal cluster accounting for 90.2% of isolates. Only two other sequence types (with variants) were identified, ST5 and ST23. ST23 was only observed in the Otago area, whereas ST5 was limited to two geographically non-contiguous areas. The sequence types are all from the enterobacterial repetitive intergenic consensus I (ERIC I) genogroup. The ST18 and ST5 from New Zealand and international P. larvae all clustered by sequence type. Based on core genome MLST and SNP analysis, localized regional clusters were observed within New Zealand, but some closely related genomes were also geographically dispersed, presumably due to hive movements by beekeepers.

Mixed-species assemblages and disease: the importance of differential vector and parasite attraction in transmission dynamics.

Individuals from multiple species often aggregate at resources, group to facilitate defense and foraging, or are brought together by human activity. While it is well-documented that host-seeking disease vectors and parasites show biases in their responses to cues from different hosts, the influence of mixed-species assemblages on disease dynamics has received limited attention. Here, we synthesize relevant research in host-specific vector and parasite bias. To better understand how vector and parasite biases influence infection, we provide a conceptual framework describing cue-oriented vector and parasite host-seeking behaviour as a two-stage process that encompasses attraction of these enemies to the assemblage and their choice of hosts once at the assemblage. We illustrate this framework, developing a case study of mixed-species frog assemblages, where frog-biting midges transmit trypanosomes. Finally, we present a mathematical model that investigates how host species composition and asymmetries in vector attraction modulate transmission dynamics in mixed-species assemblages. We argue that differential attraction of vectors by hosts can have important consequences for disease transmission within mixed-species assemblages, with implications for wildlife conservation and zoonotic disease. This article is part of the theme issue 'Mixed-species groups and aggregations: shaping ecological and behavioural patterns and processes'.

A four-decade profile of apicultural demographics and production in New Zealand, 1980-2020.

The demand for honey and pollination services has continued to grow in many countries worldwide, including New Zealand. This has influenced changes in the demographics of the managed population of honey bees (Apis mellifera). We examined historical data to describe how the apicultural demographics in New Zealand have changed temporally and geographically in the four decades to 2020. We also describe trends in honey production and the economic value of pure honey exported from New Zealand between 2000 and 2020. Our findings suggest that commercial apiculture has been key to the intensification of beekeeping in New Zealand during the study period. This is supported by evidence showing pronounced expansion of beekeeping operations among those with more than 1,000 colonies. The intensification has resulted in the density of apiaries increasing threefold across New Zealand during the four decades. While higher numbers of colonies per area produced higher volumes of honey, there was no corresponding improvement in production efficiency. Honey yields per apiary or colony, as indicators of production efficiency, appear to decline from the mid-2000s. The volume of pure honey export increased over 40-fold, a magnitude approximately ten times higher than that of production increase. This reflects a substantial increase in returns from honey exports, mostly driven by the price of manuka honey. Our findings add to a pool of information to support evidence-based decision making to enhance honey bee health and develop the apicultural industry in New Zealand.

Approaches to long-read sequencing in a clinical setting to improve diagnostic rate.

Over the past decade, advances in genetic testing, particularly the advent of next-generation sequencing, have led to a paradigm shift in the diagnosis of molecular diseases and disorders. Despite our present collective ability to interrogate more than 90% of the human genome, portions of the genome have eluded us, resulting in stagnation of diagnostic yield with existing methodologies. Here we show how application of a new technology, long-read sequencing, has the potential to improve molecular diagnostic rates. Whole genome sequencing by long reads was able to cover 98% of next-generation sequencing dead zones, which are areas of the genome that are not interpretable by conventional industry-standard short-read sequencing. Through the ability of long-read sequencing to unambiguously call variants in these regions, we discovered an immunodeficiency due to a variant in IKBKG in a subject who had previously received a negative genome sequencing result. Additionally, we demonstrate the ability of long-read sequencing to detect small variants on par with short-read sequencing, its superior performance in identifying structural variants, and thirdly, its capacity to determine genomic methylation defects in native DNA. Though the latter technical abilities have been demonstrated, we demonstrate the clinical application of this technology to successfully identify multiple types of variants using a single test.

Varroa Appears to Drive Persistent Increases in New Zealand Colony Losses.

New Zealand's temperate climate and bountiful flora are well suited to managed honey bees, and its geographic isolation and strict biosecurity laws have made sure that some pests and diseases affecting bees elsewhere are not present. Nevertheless, given the importance of pollination and high-value export honey to the economy, New Zealand began systematically measuring winter colony losses in 2015. The New Zealand Colony Loss Survey is modelled on the COLOSS survey but has been adapted to the New Zealand apicultural context. Some 49% of New Zealand beekeepers completed the winter 2021 survey. Between 2015 and 2021, overall colony loss rates increased monotonically from 8.37% [95% CI: 7.66%, 9.15%] to 13.59% [95% CI: 13.21%, 13.99%]. Whereas beekeepers most commonly attributed losses to queen problems between 2015 and 2020, attributions to varroa have escalated year-on-year to become the largest attributed cause of colony loss. Losses to varroa are perhaps amplified by the 23.4% of respondents who did not monitor mite loads and the 4.4% of beekeepers who did not treat varroa during the 2020/21 season. Indeed, most beekeepers consider their treatment to be effective and note that treating at the wrong time and reinvasion were major drivers of losses to varroa.

Land reversion and zoonotic spillover risk.

Deforestation alters wildlife communities and modifies human-wildlife interactions, often increasing zoonotic spillover potential. When deforested land reverts to forest, species composition differences between primary and regenerating (secondary) forest could alter spillover risk trajectory. We develop a mathematical model of land-use change, where habitats differ in their relative spillover risk, to understand how land reversion influences spillover risk. We apply this framework to scenarios where spillover risk is higher in deforested land than mature forest, reflecting higher relative abundance of highly competent species and/or increased human-wildlife encounters, and where regenerating forest has either very low or high spillover risk. We find the forest regeneration rate, the spillover risk of regenerating forest relative to deforested land, and how rapidly regenerating forest regains attributes of mature forest determine landscape-level spillover risk. When regenerating forest has a much lower spillover risk than deforested land, reversion lowers cumulative spillover risk, but instaneous spillover risk peaks earlier. However, when spillover risk is high in regenerating and cleared habitats, landscape-level spillover risk remains high, especially when cleared land is rapidly abandoned then slowly regenerates to mature forest. These results suggest that proactive wildlife management and awareness of human exposure risk in regenerating forests could be important tools for spillover mitigation.

Habitat Specialization by Wildlife Reduces Pathogen Spread in Urbanizing Landscapes.

AbstractUrban areas are expanding globally with far-reaching ecological consequences, including for wildlife-pathogen interactions. Wildlife show tremendous variation in their responses to urbanization; even within a single population, some individuals can specialize on urban or natural habitat types. This specialization could alter pathogen impacts on host populations via changes to wildlife movement and aggregation. Here, we build a mechanistic model to explore how habitat specialization in urban landscapes affects interactions between a mobile host population and a density-dependent specialist pathogen that confers no immunity. We model movement on a network of resource-stable urban sites and resource-fluctuating natural sites, where hosts are urban specialists, natural specialists, or generalists that use both patch types. We find that for generalists, natural and partially urban landscapes produce the highest infection prevalence and mortality, driven by high movement rates at natural sites and high densities at urban sites. However, habitat specialization protects hosts from these negative effects of partially urban landscapes by limiting movement between patch types. These findings suggest that habitat specialization can benefit populations by reducing infectious disease transmission, but by reducing movement between habitat types it could also carry the cost of reducing other movement-related ecosystem functions, such as seed dispersal and pollination.

Recurrent transitions to Little Ice Age-like climatic regimes over the Holocene.

Holocene climate variability is punctuated by episodic climatic events such as the Little Ice Age (LIA) predating the industrial-era warming. Their dating and forcing mechanisms have however remained controversial. Even more crucially, it is uncertain whether earlier events represent climatic regimes similar to the LIA. Here we produce and analyse a new 7500-year long palaeoclimate record tailored to detect LIA-like climatic regimes from northern European tree-ring data. In addition to the actual LIA, we identify LIA-like ca. 100-800 year periods with cold temperatures combined with clear sky conditions from 540 CE, 1670 BCE, 3240 BCE and 5450 BCE onwards, these LIA-like regimes covering 20% of the study period. Consistent with climate modelling, the LIA-like regimes originate from a coupled atmosphere-ocean-sea ice North Atlantic-Arctic system and were amplified by volcanic activity (multiple eruptions closely spaced in time), tree-ring evidence pointing to similarly enhanced LIA-like regimes starting after the eruptions recorded in 1627 BCE, 536/540 CE and 1809/1815 CE. Conversely, the ongoing decline in Arctic sea-ice extent is mirrored in our data which shows reversal of the LIA-like conditions since the late nineteenth century, our record also correlating highly with the instrumentally recorded Northern Hemisphere and global temperatures over the same period. Our results bridge the gaps between low- and high-resolution, precisely dated proxies and demonstrate the efficacy of slow and fast components of the climate system to generate LIA-like climate regimes. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1007/s00382-021-05669-0.

Not just trash birds: Quantifying avian diversity at landfills using community science data.

Landfills provide seasonally reliable food resources to many bird species, including those perceived to be pest or invasive species. However, landfills often contain multiple habitat types that could attract diverse species, including those of conservation concern. To date, little is known about the characteristics and composition of bird communities at landfills relative to local and regional pools. Here we used the community science database eBird to extract avian species occurrence data at landfills across the US. We compared species richness and community similarity across space in comparison to similarly-sampled reference sites, and further quantified taxonomic and dietary traits of bird communities at landfills. While landfills harbored marginally lower species richness than reference sites (respective medians of 144 vs 160), landfill community composition, and its turnover across space, were similar to reference sites. Consistent with active waste disposal areas attracting birds, species feeding at higher trophic levels, especially gulls, were more frequently observed at landfills than reference sites. However, habitat specialists including two declining grassland species, Eastern Meadowlark (Sturnella magna) and Savannah Sparrow (Passerculus sandwichensis), as well as migratory waterfowl, were more frequently encountered at landfills than reference sites. Together, these results suggest that landfills harbor comparable avian diversity to neighboring sites, and that habitats contained within landfill sites can support species of conservation concern. As covered landfills are rarely developed or forested, management of wetlands and grasslands at these sites represents an opportunity for conservation.

Alternative transmission pathways for guinea worm in dogs: implications for outbreak risk and control.

Guinea worm (Dracunculus medinensis) has exerted a high human health burden in parts of Africa. Complete eradication of Guinea worm disease (dracunculiasis) may be delayed by the circulation of the parasite in domestic dogs. As with humans, dogs acquire the parasite by directly ingesting infected copepods, and recent evidence suggests that consuming frogs that ingested infected copepods as tadpoles may be a viable transmission route (paratenic route). To understand the relative contributions of direct and paratenic transmission routes, we developed a mathematical model that describes transmission of Guinea worm between dogs, copepods and frogs. We explored how the parasite basic reproductive number (R0) depends on parameters amenable to actionable interventions under three scenarios: frogs/tadpoles do not consume copepods; tadpoles consume copepods but frogs do not contribute to transmission; and frogs are paratenic hosts. We found a non-monotonic relationship between the number of dogs and R0. Generally, frogs can contribute to disease control by removing infected copepods from the waterbody even when paratenic transmission can occur. However, paratenic transmission could play an important role in maintaining the parasite when direct transmission is reduced by interventions focused on reducing copepod ingestion by dogs. Together, these suggest that the most effective intervention strategies may be those which focus on the reduction of copepods, as this reduces outbreak potential irrespective of the importance of the paratenic route.

Extended haplotype-phasing of long-read de novo genome assemblies using Hi-C.

Haplotype-resolved genome assemblies are important for understanding how combinations of variants impact phenotypes. To date, these assemblies have been best created with complex protocols, such as cultured cells that contain a single-haplotype (haploid) genome, single cells where haplotypes are separated, or co-sequencing of parental genomes in a trio-based approach. These approaches are impractical in most situations. To address this issue, we present FALCON-Phase, a phasing tool that uses ultra-long-range Hi-C chromatin interaction data to extend phase blocks of partially-phased diploid assembles to chromosome or scaffold scale. FALCON-Phase uses the inherent phasing information in Hi-C reads, skipping variant calling, and reduces the computational complexity of phasing. Our method is validated on three benchmark datasets generated as part of the Vertebrate Genomes Project (VGP), including human, cow, and zebra finch, for which high-quality, fully haplotype-resolved assemblies are available using the trio-based approach. FALCON-Phase is accurate without having parental data and performance is better in samples with higher heterozygosity. For cow and zebra finch the accuracy is 97% compared to 80-91% for human. FALCON-Phase is applicable to any draft assembly that contains long primary contigs and phased associate contigs.

Light pollution affects West Nile virus exposure risk across Florida.

Emerging infectious diseases (EIDs) present global health threats, and their emergences are often linked to anthropogenic change. Artificial light at night (ALAN) is one form of anthropogenic change that spans beyond urban boundaries and may be relevant to EIDs through its influence on the behaviour and physiology of hosts and/or vectors. Although West Nile virus (WNV) emergence has been described as peri-urban, we hypothesized that exposure risk could also be influenced by ALAN in particular, which is testable by comparing the effects of ALAN on prevalence while controlling for other aspects of urbanization. By modelling WNV exposure among sentinel chickens in Florida, we found strong support for a nonlinear relationship between ALAN and WNV exposure risk in chickens with peak WNV risk occurring at low ALAN levels. Although our goal was not to discern how ALAN affected WNV relative to other factors, effects of ALAN on WNV exposure were stronger than other known drivers of risk (i.e. impervious surface, human population density). Ambient temperature in the month prior to sampling, but no other considered variables, strongly influenced WNV risk. These results indicate that ALAN may contribute to spatio-temporal changes in WNV risk, justifying future investigations of ALAN on other vector-borne parasites.

Uncoupling Molecular Testing for SARS-CoV-2 From International Supply Chains.

The rapid global rise of COVID-19 from late 2019 caught major manufacturers of RT-qPCR reagents by surprise and threw into sharp focus the heavy reliance of molecular diagnostic providers on a handful of reagent suppliers. In addition, lockdown and transport bans, necessarily imposed to contain disease spread, put pressure on global supply lines with freight volumes severely restricted. These issues were acutely felt in New Zealand, an island nation located at the end of most supply lines. This led New Zealand scientists to pose the hypothetical question: in a doomsday scenario where access to COVID-19 RT-qPCR reagents became unavailable, would New Zealand possess the expertise and infrastructure to make its own reagents onshore? In this work we describe a review of New Zealand's COVID-19 test requirements, bring together local experts and resources to make all reagents for the RT-qPCR process, and create a COVID-19 diagnostic assay referred to as HomeBrew (HB) RT-qPCR from onshore synthesized components. This one-step RT-qPCR assay was evaluated using clinical samples and shown to be comparable to a commercial COVID-19 assay. Through this work we show New Zealand has both the expertise and, with sufficient lead time and forward planning, infrastructure capacity to meet reagent supply challenges if they were ever to emerge.

Urban specialization reduces habitat connectivity by a highly mobile wading bird.

BACKGROUND: Mobile animals transport nutrients and propagules across habitats, and are crucial for the functioning of food webs and for ecosystem services. Human activities such as urbanization can alter animal movement behavior, including site fidelity and resource use. Because many urban areas are adjacent to natural sites, mobile animals might connect natural and urban habitats. More generally, understanding animal movement patterns in urban areas can help predict how urban expansion will affect the roles of highly mobile animals in ecological processes. METHODS: Here, we examined movements by a seasonally nomadic wading bird, the American white ibis (Eudocimus albus), in South Florida, USA. White ibis are colonial wading birds that forage on aquatic prey; in recent years, some ibis have shifted their behavior to forage in urban parks, where they are fed by people. We used a spatial network approach to investigate how individual movement patterns influence connectivity between urban and non-urban sites. We built a network of habitat connectivity using GPS tracking data from ibis during their non-breeding season and compared this network to simulated networks that assumed individuals moved indiscriminately with respect to habitat type. RESULTS: We found that the observed network was less connected than the simulated networks, that urban-urban and natural-natural connections were strong, and that individuals using urban sites had the least-variable habitat use. Importantly, the few ibis that used both urban and natural habitats contributed the most to connectivity. CONCLUSIONS: Habitat specialization in urban-acclimated wildlife could reduce the exchange of propagules and nutrients between urban and natural areas, which has consequences both for beneficial effects of connectivity such as gene flow and for detrimental effects such as the spread of contaminants or pathogens.

Landscape-level toxicant exposure mediates infection impacts on wildlife populations.

Anthropogenic landscape modification such as urbanization can expose wildlife to toxicants, with profound behavioural and health effects. Toxicant exposure can alter the local transmission of wildlife diseases by reducing survival or altering immune defence. However, predicting the impacts of pathogens on wildlife across their ranges is complicated by heterogeneity in toxicant exposure across the landscape, especially if toxicants alter wildlife movement from toxicant-contaminated to uncontaminated habitats. We developed a mechanistic model to explore how toxicant effects on host health and movement propensity influence range-wide pathogen transmission, and zoonotic exposure risk, as an increasing fraction of the landscape is toxicant-contaminated. When toxicant-contaminated habitat is scarce on the landscape, costs to movement and survival from toxicant exposure can trap infected animals in contaminated habitat and reduce landscape-level transmission. Increasing the proportion of contaminated habitat causes host population declines from combined effects of toxicants and infection. The onset of host declines precedes an increase in the density of infected hosts in contaminated habitat and thus may serve as an early warning of increasing potential for zoonotic spillover in urbanizing landscapes. These results highlight how sublethal effects of toxicants can determine pathogen impacts on wildlife populations that may not manifest until landscape contamination is widespread.

Reactivation of latent infections with migration shapes population-level disease dynamics.

Annual migration is common across animal taxa and can dramatically shape the spatial and temporal patterns of infectious disease. Although migration can decrease infection prevalence in some contexts, these energetically costly long-distance movements can also have immunosuppressive effects that may interact with transmission processes in complex ways. Here, we develop a mechanistic model for the reactivation of latent infections driven by physiological changes or energetic costs associated with migration (i.e. 'migratory relapse') and its effects on disease dynamics. We determine conditions under which migratory relapse can amplify or reduce infection prevalence across pathogen and host traits (e.g. infectious periods, virulence, overwinter survival, timing of relapse) and transmission phenologies. We show that relapse at either the start or end of migration can dramatically increase prevalence across the annual cycle and may be crucial for maintaining pathogens with low transmissibility and short infectious periods in migratory populations. Conversely, relapse at the start of migration can reduce the prevalence of highly virulent pathogens by amplifying culling of infected hosts during costly migration, especially for highly transmissible pathogens and those transmitted during migration or the breeding season. Our study provides a mechanistic foundation for understanding the spatio-temporal patterns of relapsing infections in migratory hosts, with implications for zoonotic surveillance and understanding how infection patterns will respond to shifts in migratory propensity associated with environmental change. Further, our work suggests incorporating within-host processes into population-level models of pathogen transmission may be crucial for reconciling the range of migration-infection relationships observed across migratory species.

Identifying correlates of Guinea worm (Dracunculus medinensis) infection in domestic dog populations.

Few human infectious diseases have been driven as close to eradication as dracunculiasis, caused by the Guinea worm parasite (Dracunculus medinensis). The number of human cases of Guinea worm decreased from an estimated 3.5 million in 1986 to mere hundreds by the 2010s. In Chad, domestic dogs were diagnosed with Guinea worm for the first time in 2012, and the numbers of infected dogs have increased annually. The presence of the parasite in a non-human host now challenges efforts to eradicate D. medinensis, making it critical to understand the factors that correlate with infection in dogs. In this study, we evaluated anthropogenic and environmental factors most predictive of detection of D. medinensis infection in domestic dog populations in Chad. Using boosted regression tree models to identify covariates of importance for predicting D. medinensis infection at the village and spatial hotspot levels, while controlling for surveillance intensity, we found that the presence of infection in a village was predicted by a combination of demographic (e.g. fishing village identity, dog population size), geographic (e.g. local variation in elevation), and climatic (e.g. precipitation and temperature) factors, which differed between northern and southern villages. In contrast, the presence of a village in a spatial infection hotspot, was primarily predicted by geography and climate. Our findings suggest that factors intrinsic to individual villages are highly predictive of the detection of Guinea worm parasite presence, whereas village membership in a spatial infection hotspot is largely determined by location and climate. This study provides new insight into the landscape-scale epidemiology of a debilitating parasite and can be used to more effectively target ongoing research and possibly eradication and control efforts.